The Maintenance of Sex: Ronald Fisher meets the Red Queen

Abstract: Sex in higher diploids carries a two-fold cost of males that should reduce its fitness relative to cloning and result in its extinction. Instead, sex is widespread and it is clonal species that face early obsolescence. One possible reason is that sex is an adaptation to resist ubiquitous parasites, which evolve rapidly and potentially antagonistically. We use a heuristic approach to model mutation-selection in finite populations where a parasitic haploid mounts a negative frequency-dependent attack on a diploid host. The host evolves reflexively to reduce parasitic load. Both host and parasite populations generate novel alleles by mutation and have access to large allele spaces. Sex outcompetes cloning by two overlapping mechanisms. First, sexual diploids adopt advantageous homozygous mutations more rapidly than clonal diploids under conditions of lag load. This rate advantage can offset the lesser fecundity of sex. Second, a relative advantage to sex emerges under host mutation rates that are fast enough to retain fitness in a rapidly mutating parasite environment and increase host polymorphism. Clonal polymorphic populations disproportionately experience interference with selection at high mutation rates, both between and within loci. This slows clonal population adaptation to a changing parasite environment and reduces clonal population fitness relative to sex. The interference increases markedly with the number of loci under independent selection. Rates of parasite mutation exist that not only allow sex to survive despite the two-fold cost of males but which enable sexual and clonal populations to have equal fitness and co-exist. Since all higher organisms carry parasitic loads, the model is of general applicability.